Thoracoscopy has been used to perform several procedures in dogs, including lung lobectomy,1–9 thymoma resection,10–12 pericardiectomy,13 and thoracic duct ligation.14–16 During thoracoscopic surgery, especially for lobectomy, it is essential to obtain adequate working space for manipulation of pulmonary masses, exposure of the pulmonary hilum, and instrument maneuverability, including the opening and closing of the jaws of the linear stapler. Most previously reported thoracoscopic lobectomies have been conducted in medium- to large-breed dogs weighing ≥ 20 kg, which likely provide adequate working space.1–7,9 In small-breed dogs and cats, clinical reports of lobectomy are still limited because the smaller thorax reduces the working space and hinders surgery.6 The major limitations and challenges of thoracoscopy in both small-breed dogs and cats are typically due to the restricted working space.6,8,17,18 Other challenges pertaining to thoracoscopy are related to one-lung ventilation (OLV) and the presence of large masses or adhesions that reduce visibility.
During thoracoscopic surgery, OLV is one of the most important procedures for increasing working space. The endobronchial blocker (EBB) and double-lumen endotracheal tubes for OLV are designed for humans and are not adapted to all breeds of dogs because the trachea of dogs is longer and wider than that of humans.19,20 In many dogs, the right anterior lobe bronchus is located cranial to the tracheal bifurcation, and inflating the cuff of the blocking equipment obstructs the bronchus in this lobe, which is not ideal. Also on the left side, the primary bronchus is shorter than the cuff of the blocking equipment, which may result in additional lung blockage. Moreover, in cats and small dogs, the bronchoscope and blocking equipment are large for the size of the trachea, making establishing OLV considerably more difficult.17,19
Another technique for increasing working space is carbon dioxide insufflation (CDI) of the pleural space to a predetermined pressure.11,18,21 In veterinary surgery, CDI has been used in the resection of thymic masses in a cat.11 In human infants22 and robot-assisted thoracic surgery,23–25 OLV and CDI have been combined to increase the working space. OLV combined with CDI (OLV-CDI) has been investigated in healthy cats and has been reported to lead to a subjective increase in working space as compared with OLV alone.17 The combination of OLV-CDI has not been investigated in dogs.
The effects of OLV-CDI on cardiopulmonary function were deemed acceptable during video-assisted thoracoscopic lung lobectomy in human infants22 and robot-assisted thoracoscopic lobectomy.23,25 Concerns exist regarding OLV-CDI’s potential adverse effects on cardiopulmonary function, including worsening gas exchange efficiency leading to a greater reduction in arterial partial pressure of oxygen, compared with OLV alone. A report17 evaluating the effects of OLV-CDI on cardiopulmonary function in healthy cats suggested that a manometry-measured intrathoracic pressure of approximately 3 mm Hg could be used to limit the effects on cardiopulmonary function. The purposes of the study reported here were to evaluate the effects of OLV-CDI on intrathoracic working space (determined by means of CT) during thoracoscopy in small-breed dogs and investigate conditions that could safely improve working space compared with OLV alone. We hypothesized that OLV-CDI would increase the intrathoracic working space, compared with OLV alone, even at a low intrapleural pressure (IPP).
Materials and Methods
Dogs
Six healthy 2-year-old female Beagles (median weight, 8.9 kg; range, 8.5 to 10.0 kg) were used in the study. The sample size was selected on the basis of a previous study17 involving 6 cats. None of the dogs had any evidence of underlying disease on the basis of results of a CBC, serum biochemical profile, and thoracic radiography. All dogs were cared for and managed at our facility after completion of the study. The study protocol was reviewed and approved by the Azabu University Institutional Animal Care and Use Committee (approval No. 160804-2). All dogs were treated in accordance with standard humane treatment guidelines.
Anesthesia and analgesia
All dogs were anesthetized with the same standardized protocol. A 22-gauge IV catheter was placed in a cephalic vein. Dogs were premedicated with atropine (0.025 mg/kg, SC) and midazolam (0.2 mg/kg, IV), and anesthesia was induced with propofol (2 to 3 mg/kg, slow IV to effect). A 9.0-mm cuffed endotracheal tube was inserted. Anesthesia was maintained with isoflurane (vaporizer setting, 0% to 1%) delivered in oxygen via the endotracheal tube and a propofol constant rate infusion (0.3 to 0.7 mg/kg/min, IV). OLV was established with a 9F EBB (Arndt Endobronchial Blocker; Cook Medical Inc) under flexible bronchoscopic guidance (MAF-GM; Olympus). Bronchoscopy was performed through the tracheal tube distally to allow placement of the EBB in the right or left bronchus as needed. The EBB cuff was inflated at the level of the cranial lobe bronchus to obstruct the mainstem bronchus. Right-sided OLV (R-OLV) was defined as blockage of the left lung and ventilation of the right lung, and left-sided OLV (L-OLV) was defined as blockage of the right lung and ventilation of the left lung. Dogs were randomly assigned to the R-OLV (n = 3) or L-OLV (3) group with the RAND function of Excel (Microsoft Corp). Dogs were mechanically ventilated with a pressure-controlled respirator (Compos X; Metran Co). Baseline respiratory management consisted of an inspired fraction of oxygen > 0.95, peak inspiratory pressure of 15 to 20 cm H2O, positive end-expiratory pressure (PEEP) of 5 cm H2O, and respiratory rate of 20 breaths/min. Vecuronium bromide (0.1 mg/kg, IV) was administered as a muscle relaxant to eliminate potential spontaneous respiration during CT imaging, with additional boluses (0.04 mg/kg, IV) administered at 25-minute intervals as needed. Pain management consisted of local injection of bupivacaine (2 mg/kg) into the intercostal space where the trocar sleeve was placed and into 4 additional intercostal spaces (2 cranially and 2 caudally). All dogs received lactated Ringer solution (5 mL/kg/h, IV) throughout the procedure.
CDI
A standard technique for CDI was developed for the study. In brief, dogs were positioned in lateral recumbency with the ventilated hemithorax down. The blocked hemithorax was aseptically prepared and sterilized for trocar sleeve placement. After OLV was established, a skin incision was performed in the dorsal third of the ninth intercostal space. The SC tissue and muscle were incised, and the pleura was bluntly punctured with a mosquito forceps. A laparoscopic trocar sleeve with Luer-lock attachment for 5-mm instruments (E·Z Trocar Smart Insertion Very Short; Hakko Co) was inserted into the thorax through the incision. A 5-mm 30° thoracoscope (1588 AIM; Stryker) was then inserted through the trocar sleeve into the thoracic cavity to confirm adequate lung blockage. Carbon dioxide was insufflated via the trocar sleeve with Luer-lock attachment, creating the required pneumothorax. An IPP of 3 or 5 mm Hg was maintained with a mechanical insufflator (PneumoSure; Stryker).
CT
Dogs were positioned in lateral recumbency with the ventilated hemithorax down for CT (BrightSpeed 16; GE Healthcare). CT was performed under 3 conditions: during OLV alone, during OLV-CDI at an IPP of 3 mm Hg (OLV-CDI-3), and during OLV-CDI at an IPP of 5 mm Hg (OLV-CDI-5). All dogs underwent all 3 conditions, and the order of conditions (OLV alone, then OLV-CDI-3, and then OLV-CDI-5) was the same for all dogs. The mechanical ventilator was maintained at a PEEP of 5 cm H2O for the expiratory phase throughout the scans. Between each condition, 2-lung ventilation without OLV-CDI was performed to stabilize the dog and expand the lung. Re-expansion of the lung was confirmed by thoracoscopy. Subsequently, OLV was reestablished. During the study, anesthetic monitoring was performed with a multiparameter monitor (DS-7110; Fukuda Denshi Co). Heart rate (HR), percentage hemoglobin saturation with oxygen (Spo2), and mean arterial pressure (MAP) were recorded.
At the end of the study, 2-lung ventilation without OLV-CDI was reestablished, and the blocked lung was re-expanded as previously described. The trocar cannula was removed, and the port site was closed with simple interrupted sutures of 3-0 polydioxanone. The skin was closed with staples. Each dog was then allowed to recover from general anesthesia. The dogs underwent a physical examination 5 days after the study was completed.
Outcomes
Working space volume (WSV), ventilated space volume (VSV), and thoracic cavity volume (TCV) were measured on transverse CT images. All data were measured with standard DICOM software (Osirix, version 11.0 for Mac OS; Pixmeo). For volumetry, the corresponding regions were manually segmented on all transverse CT images between the thoracic inlet and the diaphragm on the DICOM viewer. The WSV was defined as the region inflated by CO2 in the thoracic cavity on the blocked side, the VSV was defined as the lung field on the ventilated side, and the TCV was defined as the volume delimited by the parietal pleura, including regions inflated by CO2 within the thoracic cavity and the heart, mediastinal organs, and lungs.
Statistical analysis
All data were summarized as medians and ranges. The Friedman test was used to assess the effect of ventilation condition (OLV alone vs OLV-CDI-3 vs OLV-CDI-5) on WSV, VSV, and TCV. Results of the Friedman test with a 2-sided P value < .05 were considered significant, and pairwise comparisons were performed with the Mann-Whitney U test with multiplicity adjustment.26 HR, Spo2, and MAP were all analyzed with the same tests. All data were analyzed with standard software (Prism 9; GraphPad Software).
Results
The OLV, OLV-CDI, and CT procedures were successful in all dogs (Figure 1), and the dogs recovered from general anesthesia without complications. Median WSV was significantly increased during both OLV-CDI-3 (P = .0433) and OLV-CDI-5 (P = .0015), compared with median WSV during OLV alone (Figure 2). Median VSV was significantly decreased during OLV-CDI-5 (P = .0005), compared with median VSV during OLV alone, but not during OLV-CDI-3 (P = .0833). Median TCV was significantly increased during OLV-CDI-3 (P = .0433) and OLV-CDI-5 (P = .0015), compared with median TCV during OLV alone. There were no significant differences between OLV-CDI-3 and OLV-CDI-5 in regard to WSV (P = .2482), VSV (P = .0833), or TCV (P = .2482).
Transverse CT (top row) and thoracoscopic (bottom row) images during one-lung ventilation (OLV) in a dog (A), OLV combined with carbon dioxide insufflation (OLV-CDI) at an intrapleural pressure (IPP) of 3 mm Hg (B), and OLV-CDI at an IPP of 5 mm Hg (C). Notice that during OLV alone, the mediastinum is maintained within the midline, but that the mediastinum is compressed laterally and the lung collapses during OLV-CDI.
Citation: American Journal of Veterinary Research 83, 9; 10.2460/ajvr.22.01.0009
Box-and-whisker plots of thoracic cavity volume (TCV), ventilated space volume (VSV), and working space volume (WSV) in 6 healthy Beagles during OLV alone, OLV-CDI at an intrapleural pressure (ITP) of 3 mm Hg, and OLV-CDI at an ITP of 5 mm Hg. In each plot, the box represents the interquartile range, the horizontal line in the box represents the median, and the whiskers represent the range. *Values were significantly (P < .05) different. **Values were significantly (P < .01) different. ***Values were significantly (P < .001) different.
Citation: American Journal of Veterinary Research 83, 9; 10.2460/ajvr.22.01.0009
Median Spo2 during OLV-CDI-3 was not significantly (P = .1489) lower than median Spo2 during OLV alone but was significantly (P = .0009) decreased during OLV-CDI-5 (Figure 3). During OLV-CDI-5, iatrogenic pneumothorax on the contralateral side was noted on CT images of 4 of the 6 dogs.
Box-and-whisker plots of Spo2 for the dogs in Figure 2. See Figure 2 for key.
Citation: American Journal of Veterinary Research 83, 9; 10.2460/ajvr.22.01.0009
Median HR did not differ significantly between OLV alone and OLV-CDI-3 (P = .2482) or between OLV alone and OLV-CDI-5 (P = .1489). Median MAP was not significantly different between OLV alone and OLV-CDI-3 (P = .1939) or between OLV alone and OLV-CDI-5 (P > .99).
Discussion
Results of the present study indicated the OLV-CDI caused a relative increase in WSV of 130% and 193% with IPPs of 3 and 5 mm Hg, respectively, compared with OLV alone. The TCV also increased with OLV-CDI; however, relative increases with OLV-CDI-3 and OLV-CDI-5 were only 21% and 37%, respectively, compared with OLV.
OLV-CDI is performed to increase the working space during thoracoscopic surgery. CDI achieves this effect by creating an artificial positive-pressure pneumothorax to dislocate the lung lobes and other intrathoracic organs, expanding the chest wall.18,27 The combination of OLV and CDI, which are different methods to increase the working space, has been used to maximize the outcome of infant video-assisted thoracoscopic surgery and robot-assisted thoracic surgery.22–25 It has also been reported that OLV-CDI increases the working space in healthy cats.17 In the present study, WSV increased mainly due to a decrease in VSV and displacement of the mediastinum; however, increased TCV was also a factor.
In our study, OLV-CDI-3 and OLV-CDI-5 resulted in 46% and 62% decreases in VSV, respectively, compared with OLV alone. These decreases in VSV were due to the artificial positive-pressure pneumothorax, which may affect oxygenation ability. In a report21 of 2-lung ventilation with CDI alone, the Spo2 significantly decreased at IPPs ≥ 9 mm Hg. With OLV-CDI, the blood flow within the ventilated lung is increased as a result of hypoxic pulmonary vasoconstriction in response to OLV28–30 and by the effect of gravity, since the ventilated lung is positioned inferiorly in the lateral recumbent position.27 Patients who undergo OLV and then have positive IPP are at risk of exacerbated intrapulmonary shunting of blood and ventilation-perfusion mismatching. This scenario potentially leads to reduced gas exchange efficiency and arterial hypoxemia. In the present study, the VSV was approximately halved and the Spo2 was significantly lower with OLV-CDI-5 than with OLV alone. However, there was no significant difference in Spo2 and VSV between OLV alone and OLV-CDI-3, although the P value (.0833) of the difference in VSV between OLV alone and OLV-CDI-3 was close to our cutoff, and a significant difference may have been found with a larger sample size. In addition, the OLV-CDI time in our study was short, because we only performed CT scans; a longer operative time during surgery might further decrease the Spo2 even during OLV-CDI-3.
The pressure to expand the lung is the transpulmonary pressure (on the alveolar wall of the ventilated lung); it is calculated as the difference between the alveolar pressure and the pleural pressure on the visceral pleura.31,32 An insufficient transpulmonary pressure due to increased pleural pressure causes alveolar collapse. In our study, both OLV-CDI-3 and OLV-CDI-5 tended to decrease Spo2, compared with OLV alone, although a significant difference was only found with OLV-CDI-5. We suggest that changes in transpulmonary pressure and a reduction in VSV secondary to CDI of the pleural space may have some effect on ventilation in the ventilated lung. However, because alveolar and pleural pressures were not measured in this study, the effects of CDI and PEEP on changes in transpulmonary pressures were not determined. Further research is needed on respiratory management with consideration of transpulmonary pressures when using OLV-CDI.
The canine mediastinum is fenestrated, whereas the mediastinal pleura is continuous, and the right and left pleural cavities are separated.33 Contralateral pneumothorax was noted only with an IPP of 5 mm Hg in the present study. Because the pleural membranes are extremely delicate, the mediastinal pleura may become partially damaged, forcing gas across the fenestrated mediastinum and contralateral pleural membrane.
During CDI alone, the working space cannot increase indefinitely as the intrathoracic pressure increases.18,21 In the present study, the WSV more than doubled, compared with OLV alone, during both OLV-CDI-3 and OLV-CDI-5. However, there was only a 27% increase from OLV-CDI-3 to OLV-CDI-5, with no significant (P = 0.2482) difference between the two procedures. Considering the increased working space and the oxygenation capacity obtained with OLV-CDI in dogs, an IPP of 3 mm Hg may be sufficient.
Our study did have some limitations. A small number of healthy dogs was included, and the narrow weight and size range of the animals were major shortcomings. Thus, the results may not be generalizable to dogs of different sizes. The order of the conditions was not randomized, and thus each condition might have been affected by the previous ones.
The recorded volume of the blocked lung depended on the time when the CT scan was performed after re-blocking. The time from lung blockage to CT scanning was not standardized, which was a major limitation. Furthermore, gas absorption is important, because alveolar Po2 is the main driver of hypoxic pulmonary vasoconstriction, which promotes shunting of blood shunt to unblocked lung lobes.34 Values of Spo2 in this study were affected by the residual air volume of the blocked lung and the recording time.
Because the only cardiopulmonary function variables measured in the present study were Spo2, HR, and MAP, the effect of OLV-CDI on cardiopulmonary function is not clear. Further investigation of cardiopulmonary variables, including blood gas variables, end-tidal CO2 concentration, cardiac output, and blood pressure, is needed to determine the effects of OLV-CDI on cardiopulmonary function.
The effect of the respiratory phase should also be considered in evaluation of WSV. The inspiratory phase was not evaluated in the present study. No difference in WSV related to the respiratory phase was noted during subjective observation via thoracoscopy.
In conclusion, when using OLV-CDI, we suggest using an IPP ≤ 3 mm Hg, considering the marginal difference in WSV between IPPs of 3 and 5 mm Hg and the negative effect of higher IPPs on Spo2. For clinical application of the combined procedure, the effects of oxygenation, cardiovascular variables, and maintenance time on patient safety must be considered. Future studies should include a more detailed evaluation of cardiopulmonary function before OLV-CDI, especially for ruling out the possibility of hypoxemia.
Acknowledgments
No third-party funding or support was received in connection with this study or the writing or publication of the article. The authors declare that there were no conflicts of interest.
The authors thank M. Hashiguchi, H. Nozaki, and T. Hirose for technical assistance with the experiments.
References
- 1. ↑
García F, Prandi D, Peña T, Franch J, Trasserra O, de la Fuente J. Examination of the thoracic cavity and lung lobectomy by means of thoracoscopy in dogs. Can Vet J. 1998;39(5):285–291.
- 2.
Lansdowne JL, Monnet E, Twedt DC, Dernell WS. Thoracoscopic lung lobectomy for treatment of lung tumors in dogs. Vet Surg. 2005;34(5):530–535.
- 3.
Laksito MA, Chambers BA, Yates GD. Thoracoscopic-assisted lung lobectomy in the dog: report of two cases. Aust Vet J. 2010;88(7):263–267.
- 4.
Peláez MJ, Jolliffe C. Thoracoscopic foreign body removal and right middle lung lobectomy to treat pyothorax in a dog. J Small Anim Pract. 2012;53(4):240–244.
- 5.
Mayhew PD, Hunt GB, Steffey MA, et al. Evaluation of short-term outcome after lung lobectomy for resection of primary lung tumors via video-assisted thoracoscopic surgery or open thoracotomy in medium- to large-breed dogs. J Am Vet Med Assoc. 2013;243(5):681–688.
- 6. ↑
Wormser C, Singhal S, Holt DE, Runge JJ. Thoracoscopic-assisted pulmonary surgery for partial and complete lung lobectomy in dogs and cats: 11 cases (2008-2013). J Am Vet Med Assoc. 2014;245(9):1036–1041.
- 7. ↑
Bleakley S, Duncan CG, Monnet E. Thoracoscopic lung lobectomy for primary lung tumors in 13 dogs. Vet Surg. 2015;44(8):1029–1035.
- 8. ↑
Park J, Lee HB, Jeong SM. Treatment of a giant pulmonary emphysematous cyst with primary bronchoalveolar papillary carcinoma in a Shih Tzu dog. Vet Surg. 2017;46(1):158–164.
- 9. ↑
Kanai E, Matsutani N, Hanawa R, Takagi S. Video-assisted thoracic surgery anatomical lobectomy for a primary lung tumor in a dog. J Vet Med Sci. 2019;81(11):1624–1627.
- 10. ↑
Mayhew PD, Friedberg JS. Video-assisted thoracoscopic resection of noninvasive thymomas using one-lung ventilation in two dogs. Vet Surg. 2008;37(8):756–762.
- 11. ↑
Griffin MA, Sutton JS, Hunt GB, Pypendop BH, Mayhew PD. Video-assisted thoracoscopic resection of a noninvasive thymoma in a cat with myasthenia gravis using low-pressure carbon dioxide insufflation. Vet Surg. 2016;45(S1):O28–O33.
- 12. ↑
MacIver MA, Case JB, Monnet EL, et al. Video-assisted extirpation of cranial mediastinal masses in dogs: 18 cases (2009-2014). J Am Vet Med Assoc. 2017;250(11):1283–1290.
- 13. ↑
Atencia S, Doyle RS, Whitley NT. Thoracoscopic pericardial window for management of pericardial effusion in 15 dogs. J Small Anim Pract. 2013;54(11):564–569.
- 14. ↑
Mayhew PD, Culp WTN, Mayhew KN, Morgan ODE. Minimally invasive treatment of idiopathic chylothorax in dogs by thoracoscopic thoracic duct ligation and subphrenic pericardiectomy: 6 cases (2007-2010). J Am Vet Med Assoc. 2012;241(7):904–909.
- 15.
Allman DA, Radlinsky MG, Ralph AG, Rawlings CA. Thoracoscopic thoracic duct ligation and thoracoscopic pericardectomy for treatment of chylothorax in dogs. Vet Surg. 2010;39(1):21–27.
- 16. ↑
Kanai H, Furuya M, Hagiwara K, et al. Efficacy of en bloc thoracic duct ligation in combination with pericardiectomy by video-assisted thoracoscopic surgery for canine idiopathic chylothorax. Vet Surg. 2020;49(Suppl 1):O102–O111.
- 17. ↑
Mayhew PD, Pascoe PJ, Shilo-Benjamini Y, Kass PH, Johnson LR. Effect of one-lung ventilation with or without low-pressure carbon dioxide insufflation on cardiorespiratory variables in cats undergoing thoracoscopy. Vet Surg. 2015;44(Suppl 1):15–22.
- 18. ↑
Mayhew PD, Pascoe PJ, Giuffrida MA, Mitchell J, Steffey MA, Culp WTN. Cardiorespiratory effects of variable pressure thoracic insufflation in cats undergoing video-assisted thoracic surgery. Vet Surg. 2019;48(S1):O130–O137.
- 19. ↑
Pascoe PJ, Mayhew PD. Anesthesia for thracoscopy. In: Fransson BA, Mayhew PD, eds. Small Animal Laparoscopy and Thoracoscopy. 2nd ed. American College of Veterinary Surgeons Foundation and Wiley-Blackwell; 2022:311–327.
- 20. ↑
Mayhew PD, Chohan A, Hardy BT, et al. Cadaveric evaluation of fluoroscopy-assisted placement of one-lung ventilation devices for video-assisted thoracoscopic surgery in dogs. Vet Surg. 2020;49(Suppl 1):O93–O101.
- 21. ↑
Daly CM, Swalec-Tobias K, Tobias AH, Ehrhart N. Cardiopulmonary effects of intrathoracic insufflation in dogs. J Am Anim Hosp Assoc. 2002;38(6):515–520.
- 22. ↑
Cano I, Antón-Pacheco JL, García A, Rothenberg S. Video-assisted thoracoscopic lobectomy in infants. Eur J Cardiothorac Surg. 2006;29(6):997–1000.
- 23. ↑
Dylewski MR, Ohaeto AC, Pereira JF. Pulmonary resection using a total endoscopic robotic video-assisted approach. Semin Thorac Cardiovasc Surg. 2011;23(1):36–42.
- 24.
Suda K, Nakauchi M, Inaba K, Ishida Y, Uyama I. Minimally invasive surgery for upper gastrointestinal cancer: our experience and review of the literature. World J Gastroenterol. 2016;22(19):4626–4637.
- 25. ↑
Dunning J, Elsaegh M, Nardini M, et al. Microlobectomy: a novel form of endoscopic lobectomy. Innovations (Phila). 2017;12(4):247–253.
- 26. ↑
Ravishanker N, Chi Z, Dey DK. A First Course in Linear Model Theory. 2nd ed. Chapman and Hall/CRC; 2021.
- 27. ↑
Polis I, Gasthuys F, Gielen I, et al. The effects of intrathoracic pressure during continuous two-lung ventilation for thoracoscopy on the cardiorespiratory parameters in sevoflurane anaesthetized dogs. J Vet Med A Physiol Pathol Clin Med. 2002;49(3):113–120.
- 28. ↑
Kudnig ST, Monnet E, Riquelme M, Gaynor JS, Corliss D, Salman MD. Effect of one-lung ventilation on oxygen delivery in anesthetized dogs with an open thoracic cavity. Am J Vet Res. 2003;64(4):443–448.
- 29.
Riquelme M, Monnet E, Kudnig ST, et al. Cardiopulmonary changes induced during one-lung ventilation in anesthetized dogs with a closed thoracic cavity. Am J Vet Res. 2005;66(6):973–977.
- 30. ↑
Riquelme M, Monnet E, Kudnig ST, et al. Cardiopulmonary effects of positive end-expiratory pressure during one-lung ventilation in anesthetized dogs with a closed thoracic cavity. Am J Vet Res. 2005;66(6):978–983.
- 31. ↑
Grieco DL, Chen L, Brochard L. Transpulmonary pressure: importance and limits. Ann Transl Med. 2017;5(14):285.
- 32. ↑
Loring SH, Topulos GP, Hubmayr RD. Transpulmonary pressure: the importance of precise definitions and limiting assumptions. Am J Respir Crit Care Med. 2016;194(12):1452–1457.
- 33. ↑
Mizer LA. The respiratory system. In: Hermanson JW, de Lahunta A, Evans HE, eds. Miller’s Anatomy of the Dog. 5th ed. Elsevier; 2020:582–589.
- 34. ↑
Hall JE. Pulmonary circulation, pulmonary edema, pleural fluid. In: Hall JE, ed. Guyton and Hall Textbook of Medical Physiology. 13th ed. Elsevier; 2016:509–516.
